Skeletal muscle biopsy: an important approach to exercise physiology research

Authors

DOI:

https://doi.org/10.33064/iycuaa2021844161

Keywords:

Biopsies, exercise, ethics, physiology, skeletal muscle

Abstract

Beginning in the 60s, muscle biopsies, along with biochemical studies have improved the understanding of exercise physiology. The advancement in the technique of biopsies and the development of molecular biology have allowed greater understanding about the molecular regulation of metabolism in muscle fibers and their adaptation to exercise. However, the usefulness of biopsies has been questioned by arguing that the risk of the procedure could be greater than the benefit. The aim of the present work was to review the literature on the safety and efficacy of skeletal muscle biopsy for the study of exercise. This review shows that, performed correctly and by an expert, skeletal muscle biopsy is a safe, low-risk procedure and is an effective tool for the investigation of exercise physiology.

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Author Biographies

Katya Vargas-Ortiz, Universidad de Guanajuato

Departamento de Ciencias Médicas, División de Ciencias de la Salud, Campus León

Victoriano Pérez-Vázquez, Universidad de Guanajuato

Departamento de Ciencias Médicas, División de Ciencias de la Salud, Campus León

Paulina Guadalupe Montaño-Ascencio, Universidad de Guanajuato

Departamento de Medicina y Nutrición, División de Ciencias de la Salud, Campus León

Maciste H. Macias-Cervantes, Universidad de Guanajuato

Departamento de Ciencias Médicas, División de Ciencias de la Salud, Campus León

References

• Archundia-Herrera, C., Macias-Cervantes, M., Ruiz-Munoz, B., Vargas-Ortiz, K., Kornhauser, C., & Perez-Vazquez, V. (2017). Muscle irisin response to aerobic vs HIIT in overweight female adolescents. Diabetol Metab Syndr, 9, 101. doi: 10.1186/s13098-017-0302-5

• Boyd, J. C., Simpson, C. A., Jung, M. E., & Gurd, B. J. (2013). Reducing the intensity and volume of interval training diminishes cardiovascular adaptation but not mitochondrial biogenesis in overweight/obese men. PLoS One, 8(7), e68091. doi: 10.1371/journal.pone.0068091

• Cobley, J. N., Bartlett, J. D., Kayani, A., Murray, S. W., Louhelainen, J., Donovan, T., . . . Close, G. L. (2012). PGC-1alpha transcriptional response and mitochondrial adaptation to acute exercise is maintained in skeletal muscle of sedentary elderly males. Biogerontology, 13(6), 621-631. doi: 10.1007/s10522-012-9408-1

• Charriere, M., & Duchenne, G.B. (1865). Emporte piece histologique. Bull Acad Med, 30, 1050-1051.

• Derry, K. L., Nicolle, M. N., Keith-Rokosh, J. A., & Hammond, R. R. (2009). Percutaneous muscle biopsies: review of 900 consecutive cases at London Health Sciences Centre. Can J Neurol Sci, 36(2), 201-206. doi: 10.1017/s0317167100006569

• Dumke, C. L., Mark Davis, J., Angela Murphy, E., Nieman, D. C., Carmichael, M. D., Quindry, J. C., . . . McAnulty, L. S. (2009). Successive bouts of cycling stimulates genes associated with mitochondrial biogenesis. Eur J Appl Physiol, 107(4), 419-427. doi: 10.1007/s00421-009-1143-1

• Edgett, B. A., Bonafiglia, J. T., Baechler, B. L., Quadrilatero, J., & Gurd, B. J. (2016). The effect of acute and chronic sprint-interval training on LRP130, SIRT3, and PGC-1alpha expression in human skeletal muscle. Physiol Rep, 4(17). doi: 10.14814/phy2.12879

• Edgett, B. A., Hughes, M. C., Matusiak, J. B., Perry, C. G., Simpson, C. A., & Gurd, B. J. (2016). SIRT3 gene expression but not SIRT3 subcellular localization is altered in response to fasting and exercise in human skeletal muscle. Exp Physiol, 101(8), 1101-1113. doi: 10.1113/ep085744

• Elder, G. C., Bradbury, K., & Roberts, R. (1982). Variability of fiber type distributions within human muscles. J Appl Physiol Respir Environ Exerc Physiol, 53(6), 1473-1480. doi: 10.1152/jappl.1982.53.6.1473

• Evans, W. J., Phinney, S. D., & Young, V. R. (1982). Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc, 14(1), 101-102.

• Gillen, J. B., Percival, M. E., Skelly, L. E., Martin, B. J., Tan, R. B., Tarnopolsky, M. A., & Gibala, M. J. (2014). Three minutes of all-out intermittent exercise per week increases skeletal muscle oxidative capacity and improves cardiometabolic health. PLoS One, 9(11), e111489. doi: 10.1371/journal.pone.0111489

• Gunnarsson, T. P., Christensen, P. M., Holse, K., Christiansen, D., & Bangsbo, J. (2012). Effect of additional speed endurance training on performance and muscle adaptations. Med Sci Sports Exerc, 44(10), 1942-1948. doi: 10.1249/MSS.0b013e31825ca446

• Gurd, B. J., Yoshida, Y., McFarlan, J. T., Holloway, G. P., Moyes, C. D., Heigenhauser, G. J., . . . Bonen, A. (2011). Nuclear SIRT1 activity, but not protein content, regulates mitochondrial biogenesis in rat and human skeletal muscle. Am J Physiol Regul Integr Comp Physiol, 301(1), R67-75. doi: 10.1152/ajpregu.00417.2010

• Henriksson, K. G. (1979). "Semi-open" muscle biopsy technique. A simple outpatient procedure. Acta Neurol Scand, 59(6), 317-323.

• Hey-Mogensen, M., Hojlund, K., Vind, B. F., Wang, L., Dela, F., Beck-Nielsen, H., . . . Sahlin, K. (2010). Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia, 53(9), 1976-1985. doi: 10.1007/s00125-010-1813-x

• Highstead, R. G., Tipton, K. D., Creson, D. L., Wolfe, R. R., & Ferrando, A. A. (2005). Incidence of associated events during the performance of invasive procedures in healthy human volunteers. J Appl Physiol (1985), 98(4), 1202-1206. doi: 10.1152/japplphysiol.01076.2004

• Holloszy, J. O. (1967). Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem, 242(9), 2278-2282.

• Hughes, M. C., Ramos, S. V., Turnbull, P. C., Nejatbakhsh, A., Baechler, B. L., Tahmasebi, H., . . . Perry, C. G. (2015). Mitochondrial Bioenergetics and Fiber Type Assessments in Microbiopsy vs. Bergstrom Percutaneous Sampling of Human Skeletal Muscle. Front Physiol, 6, 360. doi: 10.3389/fphys.2015.00360

• Item, F., Nocito, A., Thony, S., Bachler, T., Boutellier, U., Wenger, R. H., & Toigo, M. (2013). Combined whole-body vibration, resistance exercise, and sustained vascular occlusion increases PGC-1alpha and VEGF mRNA abundances. Eur J Appl Physiol, 113(4), 1081-1090. doi: 10.1007/s00421-012-2524-4

• Iversen, N., Krustrup, P., Rasmussen, H. N., Rasmussen, U. F., Saltin, B., & Pilegaard, H. (2011). Mitochondrial biogenesis and angiogenesis in skeletal muscle of the elderly. Exp Gerontol, 46(8), 670-678. doi: 10.1016/j.exger.2011.03.004

• Kazior, Z., Willis, S. J., Moberg, M., Apro, W., Calbet, J. A., Holmberg, H. C., & Blomstrand, E. (2016). Endurance Exercise Enhances the Effect of Strength Training on Muscle Fiber Size and Protein Expression of Akt and mTOR. PLoS One, 11(2), e0149082. doi: 10.1371/journal.pone.0149082

• Levett, D. Z., Vigano, A., Capitanio, D., Vasso, M., De Palma, S., Moriggi, M., . . . Gelfi, C. (2015). Changes in muscle proteomics in the course of the Caudwell Research Expedition to Mt. Everest. Proteomics, 15(1), 160-171. doi: 10.1002/pmic.201400306

• Lexell J. (1993). Ageing and human muscle: observations from Sweden. Can J Appl Physiol., 18(1), 2-18.

• Lexell J, Taylor CC. (1991). Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age. J Anat, 174, 239-249.

• Lexell, J., Henriksson-Larsen, K., & Sjostrom, M. (1983). Distribution of different fibre types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand, 117(1), 115-122. doi: 10.1111/j.1748-1716.1983.tb07185.x

• Little, J. P., Safdar, A., Bishop, D., Tarnopolsky, M. A., & Gibala, M. J. (2011). An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol, 300(6), R1303-1310. doi: 10.1152/ajpregu.00538.2010

• Little, J. P., Safdar, A., Cermak, N., Tarnopolsky, M. A., & Gibala, M. J. (2010). Acute endurance exercise increases the nuclear abundance of PGC-1alpha in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol, 298(4), R912-917. doi: 10.1152/ajpregu.00409.2009

• Macías-Cervantes, M.H., Guzmán-Flores, J.M., Vargas-Ortiz, K., Díaz-Cisneros, F.J., Ramírez-Emiliano, J., & Pérez-Vázquez, V. (2014). Effect of Aerobic Exercise on Protein Expression in Muscle of Obese Mexican Adolescents: A Proteomic and Bioinformatic Analysis. Natural Science, 6(9), 641-650.

• Neves, M., Jr., Barreto, G., Boobis, L., Harris, R., Roschel, H., Tricoli, V., . . . Gualano, B. (2012). Incidence of adverse events associated with percutaneous muscular biopsy among healthy and diseased subjects. Scand J Med Sci Sports, 22(2), 175-178. doi: 10.1111/j.1600-0838.2010.01264.x

• Paoli, A., Pacelli, Q. F., Toniolo, L., Miotti, D., & Reggiani, C. (2010). Latissimus dorsi fine needle muscle biopsy: a novel and efficient approach to study proximal muscles of upper limbs. J Surg Res, 164(2), e257-263. doi: 10.1016/j.jss.2010.05.043

• Perry, C. G., Kane, D. A., Herbst, E. A., Mukai, K., Lark, D. S., Wright, D. C., . . . Holloway, G. P. (2012). Mitochondrial creatine kinase activity and phosphate shuttling are acutely regulated by exercise in human skeletal muscle. J Physiol, 590(21), 5475-5486. doi: 10.1113/jphysiol.2012.234682

• Phielix, E., Meex, R., Moonen-Kornips, E., Hesselink, M. K., & Schrauwen, P. (2010). Exercise training increases mitochondrial content and ex vivo mitochondrial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia, 53(8), 1714-1721. doi: 10.1007/s00125-010-1764-2

• Pilegaard, H., Saltin, B., & Neufer, P. D. (2003). Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol, 546(Pt 3), 851-858. doi: 10.1113/jphysiol.2002.034850

• Psilander, N., Frank, P., Flockhart, M., & Sahlin, K. (2013). Exercise with low glycogen increases PGC-1alpha gene expression in human skeletal muscle. Eur J Appl Physiol, 113(4), 951-963. doi: 10.1007/s00421-012-2504-8

• Psilander, N., Wang, L., Westergren, J., Tonkonogi, M., & Sahlin, K. (2010). Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol, 110(3), 597-606. doi: 10.1007/s00421-010-1544-1

• Ringholm, S., Bienso, R. S., Kiilerich, K., Guadalupe-Grau, A., Aachmann-Andersen, N. J., Saltin, B., . . . Pilegaard, H. (2011). Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am J Physiol Endocrinol Metab, 301(4), E649-658. doi: 10.1152/ajpendo.00230.2011

• Saleem, A., Carter, H. N., Iqbal, S., & Hood, D. A. (2011). Role of p53 within the regulatory network controlling muscle mitochondrial biogenesis. Exerc Sport Sci Rev, 39(4), 199-205. doi: 10.1097/JES.0b013e31822d71be

• Saltin, B., & Gollnick, P. D. (2011). Skeletal Muscle Adaptability: Significance for Metabolism and Performance. Handbook of Physiology, Skeletal Muscle, 27, 1. doi: https://doi.org/10.1002/cphy.cp100119

• Scarpulla, R. C. (2011). Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta, 1813(7), 1269-1278. doi: 10.1016/j.bbamcr.2010.09.019

• Scribbans, T. D., Edgett, B. A., Vorobej, K., Mitchell, A. S., Joanisse, S. D., Matusiak, J. B., . . . Gurd, B. J. (2014). Fibre-specific responses to endurance and low volume high intensity interval training: striking similarities in acute and chronic adaptation. PLoS One, 9(6), e98119. doi: 10.1371/journal.pone.0098119

• Shanely, R. A., Zwetsloot, K. A., Triplett, N. T., Meaney, M. P., Farris, G. E., & Nieman, D. C. (2014). Human skeletal muscle biopsy procedures using the modified Bergstrom technique. J Vis Exp(91), 51812. doi: 10.3791/51812

• Skovgaard, C., Brandt, N., Pilegaard, H., & Bangsbo, J. (2016). Combined speed endurance and endurance exercise amplify the exercise-induced PGC-1alpha and PDK4 mRNA response in trained human muscle. Physiol Rep, 4(14). doi: 10.14814/phy2.12864

• Tam, E., Bruseghini, P., Calabria, E., Dal Sacco, L., Doria, C., Grassi, B., . . . Capelli, C. (2016). Gokyo Khumbu/Ama Dablam Trek 2012: effects of physical training and high-altitude exposure on oxidative metabolism, muscle composition, and metabolic cost of walking in women. Eur J Appl Physiol, 116(1), 129-144. doi: 10.1007/s00421-015-3256-z

• Tarnopolsky, M. A., Pearce, E., Smith, K., & Lach, B. (2011). Suction-modified Bergstrom muscle biopsy technique: experience with 13,500 procedures. Muscle Nerve, 43(5), 717-725. doi: 10.1002/mus.21945

• Uguccioni, G., D'Souza, D., & Hood, D. A. (2010). Regulation of PPARgamma Coactivator-1alpha Function and Expression in Muscle: Effect of Exercise. PPAR Res, 2010. doi: 10.1155/2010/937123

• Vargas-Ortiz, K., Perez-Vazquez, V., Diaz-Cisneros, F. J., Figueroa, A., Jimenez-Flores, L. M., Rodriguez-DelaRosa, G., & Macias, M. H. (2015). Aerobic Training Increases Expression Levels of SIRT3 and PGC-1alpha in Skeletal Muscle of Overweight Adolescents Without Change in Caloric Intake. Pediatr Exerc Sci, 27(2), 177-184. doi: 10.1123/pes.2014-0112

• Vincent, G., Lamon, S., Gant, N., Vincent, P. J., MacDonald, J. R., Markworth, J. F., . . . Hickey, A. J. (2015). Changes in mitochondrial function and mitochondria associated protein expression in response to 2-weeks of high intensity interval training. Front Physiol, 6, 51. doi: 10.3389/fphys.2015.00051

• Viru, A., & Viru, M. . (2003). Análisis y control del rendimiento deportivo. Barcelona: Paidotribo.

• Wens, I., Dalgas, U., Vandenabeele, F., Verboven, K., Hansen, D., Deckx, N., . . . Eijnde, B. O. (2017). High Intensity Aerobic and Resistance Exercise Can Improve Glucose Tolerance in Persons With Multiple Sclerosis: A Randomized Controlled Trial. Am J Phys Med Rehabil, 96(3), 161-166. doi: 10.1097/phm.0000000000000563

• Wilmore, J.H., & Costill, D.L. (1999). Physiology of sport and exercise (Human Kinetics Ed.). United States.

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2021-10-31

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